The orthodontic-endodontic interface: trauma and pulpal considerations

The interpretation of the clinical signs and symptoms arising from the interdisciplinary relationship between orthodontics and endodontics becomes more complicated when superimposed by dental trauma. A history of dental trauma before or during orthodontic tooth movement may have implications for pulpal health and clinical outcomes. An understanding of the biology is essential for appropriate treatment planning. This review and treatment recommendations will assist dental practitioners in managing orthodontic-endodontic interactions.


Introduction
An appreciation of the biological basis and implications of the relationships between the disciplines of orthodontics and endodontics is important for dental practitioners.Previous reviews have covered a variety of different interactions, 1,2 but the two more complex relationships are the orthodontic management of traumatised teeth and the pulpal response to orthodontic tooth movement (OTM).This narrative review will explore the biological and mechanical aspects of the relationship between OTM, dental trauma and the pulp; it is based on a recent review of a variety of topics, including pulp biology, tooth resorptions, root-filled teeth, traumatised teeth, endodontic treatment during orthodontics and OTM during endodontic treatment. 2

Orthodontics and dental trauma
Loss of pulp vitality, root resorption and pulp canal calcification (PCC) have been identified as the main risks of OTM for teeth with a history of trauma. 3These risks are reviewed below.

Pulp necrosis
Early literature reported a link between OTM and pulp necrosis of teeth with a history of dental trauma, 4,5,6 and two systematic reviews reached the same conclusion. 7,8However, other reviews reported that there was no such evidence. 9,10,11Of the main studies that reported an increased risk, 12,13,14,15,16 Brin et al. 12 based their conclusion only on the non-response to electric pulp tests and hence the diagnosis of loss of vitality is doubtful.On the other hand, in the research by Bauss et al., 13,14,15,16 the criteria included loss of pulpal sensibility, grey discolouration and periapical radiolucency.These authors concluded that traumatised maxillary incisors with severe periodontal injuries were more susceptible to pulp necrosis than non-traumatised teeth after intrusive orthodontic forces. 14A similar conclusion was reported for intrusive OTM in teeth traumatised during OTM, 15 traumatised teeth undergoing extrusive OTM, 16 and teeth with total PCC. 13The authors also hypothesised that a history of previous severe periodontal ligament (PDL) damage may somehow have resulted in teeth being less resistant to extrusive OTM due to impaired pulpal blood flow, and therefore light orthodontic forces were indicated. 16n summary, while some reviews report insufficient evidence of increased risk of pulp necrosis with OTM of traumatised teeth, 9,10,11 those reviews were based on literature with significant methodological problems. 2,7,17Therefore, there is indeed some evidence to suggest that a history of previous trauma may predispose a tooth to pulpal necrosis after OTM and it may be influenced by the type and severity of orthodontic forces. 13,14,15,16etrospectively assessed the prevalence and extent of root resorption in 55 incisor teeth in 27 patients aged 7-15 years with a previous history of 'slight or moderate' trauma.From intraoral radiographs before and after OTM, signs of root resorption of the teeth were classified based on a resorption index (Fig. 1).The authors concluded that slight or moderate dental injuries did not have a greater risk of root resorption than uninjured teeth and there was no difference between the types of mild-moderate injury. 27urther, previously traumatised teeth with signs of apical root resorption before OTM may be more prone to root resorption during treatment. 26,27n a large study of 2,451 maxillary incisors in 719 young orthodontic patients, the average loss of root length for the traumatised teeth (type and severity not specified) was 1.07 ± 1.19 mm compared with 0.64 ± 1.04 mm for the nontraumatised teeth. 28While the accuracy of the measurements and the uncertainty of the trauma history were limitations, the amount of resorption was not clinically significant.In a subsequent study on 485 of those 719 patients, 29 the authors confirmed that a history of trauma more than one year before the OTM was the most important predictor of apical root resorption, albeit that the precise trauma history was unknown.
Brin et al. 12 reported that moderate root resorption (Grades 1-2 of the Malmgren et al. classification) 27 was observed in 27.8% of previously traumatised teeth compared with 7.8% in the OTM-only group and 6.7% in the trauma-only group.A study in young patients reported no statistically significant correlation between a history of trauma and apical root resorption. 30However, pausing OTM for 2-3 months resulted in significantly less resorption (0.4 ± 0.7 mm) than continuous OTM (1.5 ± 0.8 mm). 30nother study assessed the effect of different orthodontic archwire sequences on apical root resorption and reported that a history of incisor tooth trauma did not increase the risk of resorption. 31However, the sample sizes in that study were small and the authors warned that the results were not compelling. 31everal other recent studies have also reported a lack of a convincing relationship between apical root resorption and a history of trauma subsequent to OTM, mainly due to unreliable data as reported by the authors. 32,33,34,35,36Importantly, the Malmgren index based on two-dimensional radiographs may not be accurate for cone beam computed tomography (CBCT) imaging. 33Also, case reports on the effect of OTM on traumatised immature teeth after apexification or treated with regenerative endodontic procedures, showed no increased predisposition to apical root resorption. 37,38,39,40,41Instead, the teeth were more at risk of pulp necrosis or different types of root resorption.However, the knowledge base relating to this novel trauma literature is very limited at this time.
Overall, the literature in this area suffers from small sample sizes, large standard deviations, lack of information on the intensity, location and type of trauma, potentially inaccurate measurement methods of the root lengths, and relatively short timeframes of the assessments.Recent reviews have identified a broad range of variables that may potentially affect the relationship between root resorption and OTM. 42,43Notwithstanding these issues, it appears that there is no convincing evidence to indicate that teeth with a history of trauma are routinely at greater risk of apical root resorption after OTM.The evidence supporting this contention demonstrated clinically non-significant degrees of resorption and it may relate to more severe forms of trauma, particularly affecting the PDL.However, pre-OTM evidence of apical root resorption may be predictive of an increased risk of apical root resorption during OTM.

Pulp canal calcification
The term pulp canal calcification (PCC) reflects a more accurate radiographic representation of the biological process than the term pulp canal obliteration. 2Historically, 'calcified obliteration of the pulp-chamber' was first reported in 1905. 44However, complete calcification of the pulp chamber subsequent to trauma and OTM was first reported in 1950. 45Another case report 46 showed complete calcification of a replanted iatrogenically avulsed immature mandibular premolar.In 1966, Andreasen and Hjørting-Hansen 47 published a landmark paper on the outcomes of 110 replanted teeth including 13 immature incisors, of which seven showed gradual 'obliteration' of the pulp chamber.This gradual calcification was attributed to 'pulpal damage' that Andreasen 48 later described as an 'accelerated speed of dentine deposition' , resulting in either partial or total calcification. 49The calcification was suggested to be a sequel to revascularisation and/or reinnervation of the entire traumatised pulp or parts of it. 50,51A recent literature review discusses the possible mechanisms leading to PCC. 2 Pulp necrosis subsequent to PCC is an uncommon complication, with a prevalence in the range of 1-27.2% 52,53 over observation periods of 3.4-16 years, 53 This prevalence seems to increase over time. 48,54,55Possibly because of the continuing PCC, subsequent injuries may sever the vascular supply at the narrowing apical foramen. 48New injuries to the pulp in a tooth with PCC may be in the form of restorative procedures or direct trauma. 54,55Another suggested cause was orthodontic treatment, 56 possibly due to the greater risk of damage to the vascular supply during OTM, 13,15 which may be considered to be a controlled 57 or subtle 58 form of trauma to teeth.The evidence linking PCC to OTM is discussed below.

Radiographic evidence
Delivanis and Sauer 59 questioned whether PCC was an iatrogenic side effect of orthodontic treatment or simply an isolated problem.Of 46 patients studied, only two showed PCC after OTM and both were subjected to heavy OTM forces or OTM over a very long period of time.Despite this evidence, the authors cautiously concluded that the possibility of PCC should be closely monitored in patients undergoing OTM or those in retention.On the other hand, another study 60 reported that PCC was radiographically more prevalent in orthodontic patients (17%) than in a control group (8%); although, there were no details provided concerning a trauma history or other treatment details.In another early radiographic study, Popp et al. 57 observed evidence of PCC in incisor teeth of patients in both the experimental and control groups.They interpreted this as a normal ageing process, which may have been due either to rest periods of the OTM allowing tissue repair, or that the forces were within physiological limits.However, a study on palatally impacted canines concluded that excessive OTM resulted in PCC. 61Three retrospective studies reported significant increases of 2.2%, 62 4% 63 and 22% 64 in the prevalence of pulp stones in teeth after OTM; although, the studies lacked control groups and were based on panoramic radiographs.A novel CBCT study reported a significant decrease in pulp volume of maxillary anterior teeth after some 18 months of OTM. 65The initial pulp volumes ranged from 38.12-51.02mm 3 with mean volume losses after OTM varying from 3.04-3.86mm 3 .More recent literature concluded that OTM significantly increased the prevalence of pulp stones and pulp calcification. 66,67,68In one study, there was a significant increase in the number of pulp stones of some 14% compared with 3% for the non-OTM group. 66he other studies reported a 38% increase in the number of pulp stones in the post-OTM treatment radiographs 67 and a prevalence of pulp stones and PCC in molars of some 42%. 68

Histological evidence
In an early study, orthodontic intrusion was not linked to the frequency of pulp stones in children; although, the research protocol lacked standardisation of the forces and the number of days over which the forces were applied. 69Several other histological studies 70,71,72 reported varying findings depending on the degree and duration of applied forces, which indicated an inconsistent relationship between OTM forces, timeframes and prevalence of pulp calcifications.When calcification was present, in the coronal pulp it appeared as discrete and concentric pulp stones, but in the radicular pulp was more diffuse. 71hen the pulp calcifications were large and numerous, they could occupy part or all of the pulp cavity. 71Therefore, it is feasible that the continued growth of the calcifications could lead to their coalescence resulting in PCC radiographically.Mild to moderate trauma can result in dystrophic calcification which may result in PCC unless the pulp becomes completely necrotic (Fig. 2).However, the exact mechanism by which pulp calcifications coalesce is unclear and is complicated by the different types of pulp stones and calcifications identified histologically. 73n summary, recent review papers indicate that OTM can increase PCC in nontraumatised teeth to a greater extent than that related to physiological ageing. 74,75,76,77he differences reported in the literature probably relate to variables including a history of trauma, factors related to OTM (type, duration, force levels and force vectors) and genetic predisposition. 68If pulp necrosis occurs in such teeth, endodontic treatment is feasible using contemporary endodontic protocols. 73,78,79However, if the presenting complaint is only tooth discolouration, then external bleaching strategies can be implemented. 78,79,80

Orthodontic effects on the vital pulp
The literature review above has established that a history of previous trauma and/ or PCC may predispose a tooth to pulpal necrosis after OTM. 13,14,15,16Further, because of continuing PCC, subsequent injuries, including OTM, 13,15,56 may affect or sever the vascular supply at the narrowing apical foramen. 48,55Additionally, Andreasen 48 speculated that the pulp vessels at the apical foramen may be 'strangulated' due to continued hard tissue formation.This should not be confused with the disproven 'strangulation theory' of pulp necrosis subsequent to pulpal inflammation; 81 rather, it could be considered as a compressive obstructive affect.Hence, a brief discussion of the physiological and anatomical effects of OTM on the pulp are important.

Physiological effects
Orthodontic forces have been reported to cause a wide range of physiological effects on the pulp. 2 These include initial decreased pulpal blood flow; reactive hyperaemia; a large and coordinated sprouting of pulpal blood vessels and nerve endings; vascular dilation and congestion; increased pulpal cellular responses; pulpal fibrosis and calcifications; odontoblast aspiration and disruption of the odontoblast layer; vacuolisation; vascular degeneration; interference with pulpal sensibility; increase in the expression or activity levels of certain enzymes and neuropeptides associated with inflammation; as well as reversible pulpitis. 2imilarly, a series of recent systematic reviews came to the same conclusions. 7,8,17,74,75,76,82,83mportantly, these responses appeared to be temporary and transient, and usually reversible 74,75,76,82,83 if the forces were within the physiological limits for the particular clinical situation. 75,84,85A systematic review 83 concluded that OTM did not routinely cause pulpal necrosis; although, other potential co-factors were not evaluated in the review, including a history of trauma and PCC.Consequently, the authors recommended the application of 'low' orthodontic forces. 83A vital pulp traumatised during OTM may manifest clinically as a grey discolouration but with an appropriate rest period may subsequently survive (Fig. 3).
However, despite the above documented adverse pulpal effects of OTM, there is no evidence that the reduction of blood flow is force-dependent. 7,82Nevertheless, it is feasible that the duration, magnitude, vectors and type (especially intrusion) 69,75,76,86 of OTM would increase the risks to a pulp, 80,87 particularly when compromised by other factors such as age, 88,89 which reflects the anatomical influence of a decrease in natural apical foramen size and canal dimensions due to progressive calcification.

Anatomical aspects
Almost a century ago, Coolidge 90 reported that the pulp tissue of a tooth entered the root canal in a large bundle of blood vessels, nerves and connective tissue.This arrangement of the neurovascular bundle (NVB) being continuous between the root canal space and the periapical tissues has been confirmed in subsequent research using contemporary histological techniques (Fig. 4). 91,92While the complexity of the apical root canal anatomy is implied in histological specimens (Fig. 5), three dimensional anatomical studies demonstrate

years (top right). Photographs on presentation (bottom left) and at five-month review (bottom right). Images courtesy of Dr Vijay John
the tortuous and variable nature of the root canal system of teeth, especially at the apical terminus (Fig. 6). 93uch anatomical evidence indicates that the apical foramina vary in size, shape and location, which implies that OTM will result in different force vectors and magnitudes on the NVBs at each foramen of each individual root canal of each individual tooth.Anatomical variations of the apical foramen or the NVB may explain variations in pulpal responses with OTM. 16,94Horizontal forces acting on the root apices of tooth roots during OTM may result in the NVB exerting pressure on one side of the apical foramen leading to root resorption in that region. 95Then, on the opposite side of the root apex, cementum may be laid down, with an overall effect of the apical foramen being relocated (Fig. 7). 95However, this will depend on the position of the apical foramina, so it is unlikely that all teeth will be affected in exactly the same way.Nevertheless, such images (Fig. 4, Fig. 5, Fig. 6, Fig. 7) allow us to visualise the various apical displacement forces and vectors acting on the apical NVB leading to compression or stretching of the blood vessels and the initial reduction in the blood flow, ultimately compensated for by the reactive hyperaemia. 69,96nother effect of the apical pressure or tension during OTM is the reported increase in response threshold to electric pulp testing. 97his may relate to the anatomical relationship between the apical foramen and the NVB, or it may be due to hypoxia of the pulpal Aδ fibres. 97owever, sensibility testing with cold seems not to be affected, 97,98 for which there is currently no explanation.

Recommendations
The clinically relevant question arising from the interactions between dental trauma and orthodontic treatment relates to the timing of orthodontic treatment for teeth with a history of trauma.This includes clinical scenarios where the trauma has occurred before the commencement of a course of orthodontic care, or where the trauma occurs during the OTM.While it is known that repair of resorptive defects due to OTM occurs rapidly after cessation of forces in teeth with no history of trauma, 99,100,101 intermittent 52,53,102,103,104,105,106,107 and light 2,16,20,57 orthodontic forces may minimise root resorption and pulpal complications.Unfortunately, this available literature is vague and variable in how long the delay period should be before commencing or re-commencing OTM, with a broad range of rest periods suggested for non-trauma influenced OTM.
Because of the many variables identified in the literature, 2,23 it is unlikely that a definitive rest period will ever be recommended.When there is a history of dental trauma, deciding on an appropriate rest period (also known as delay, pause, or waiting periods) is further complicated by the extent and severity of the trauma.However, timing of appropriate rest periods can allow OTM to proceed without  92 further compromise to the traumatised teeth (Fig. 8, Fig. 9, Fig. 10).An additional factor has been the use of clear aligners as an alternative to fixed orthodontic appliances with expanding clinical indications. 108Currently, there is no published literature relating outcomes of OTM with clear aligners to a history of dental trauma.However, one study confirmed that initial blood flow changes with clear aligners and fixed appliances eventually return to normal values after OTM with no difference between these two treatment modalities. 109While no randomised controlled trials exist, the available evidence indicates that orthodontically induced apical root resorption related to clear aligner treatment is unlikely to be more problematic than with fixed appliance treatment. 110,111,112onsequently, while it is reasonable to suggest that clear aligners are unlikely to be a risk for teeth with a history of dental trauma, further research in this area is required.
Furthermore, while the degree of trauma sustained is recognised as an important variable, 15 the degrees of dental trauma injuries are not clearly defined within the literature.Rather than attempting to classify into vague groups such as 'mild' , 'moderate' , or 'severe' , rest period recommendations should recognise a continuum of trauma possibilities with no definitive discriminators. 2herefore, logically, the decision should be based on the biology of the healing responses of the tissues involved (ie pulp and PDL), and also the type of trauma sustained.In cases of multiple types of trauma (Fig. 8, Fig. 9), rest periods should be based on the most severe of the injuries, generally those compromising the PDL.Histologically, pulp healing is reported to occur within some 1-3 months, 113 which becomes evident radiographically after approximately 3-6 months. 114,115However, periodontal healing involves three phases ie: 1) blood coagulation and inflammation; 2) new tissue formation; and 3) tissue remodelling. 116,117Crucially, while initial healing with type III collagen occurs within two weeks, tissue remodelling to return the periodontal tissues to their pre-wounded state, replacing the randomly-oriented type III collagen with the more organised and crosslinked type I collagen, can take at least one year. 116,117ence, the recommendations in Table 1 are based not only on previously published guidelines, 9,10,11,23,118,119 but also on the biological influences of pulpal and periodontal tissues discussed above.

Conclusions
The existing literature base confirms that there are biologically relevant interactions between orthodontics and endodontics, especially when impacted by dental trauma.This review has identified the pulpal and periodontal consequences of trauma and the effects of OTM on these interactions.The broad heterogeneity of the existing literature base is evident, complicating definitive conclusions without continued research to add to the understanding of orthodontic-endodontic interface.
Generally, during OTM, traumatised teeth appear to be more susceptible to pulpal and periapical changes, but the responses of these tissues will depend on the type and the continuum of trauma severity possibilities, as well as the variability of the factors related to OTM.When a dental injury is sustained before or during OTM, the orthodontic rest period depends on the severity of the injury, and bestavailable evidence-based guidelines should be followed.Teeth with radiographic evidence of trauma-induced inflammatory root resorption (await radiographic evidence of root and bone healing)

Fig. 2
Fig. 2 Histological section of pulp from a maxillary incisor tooth with a history of luxation followed several weeks later by avulsion and immediate replantation.Pathology report indicated 'collections of microorganisms in coccal and filamentous forms.Dystrophic calcification of varying sizes throughout the necrotic tissue.Necrotic infected pulp' (H&E x 33).Reproduced from Parashos P, 'Endodontic-orthodontic interactions: a review and treatment recommendations' Australian Dental Journal, Vol 68, 2023, Wiley 2

Fig. 4 92 Fig. 5
Fig. 4 Root apex and surrounding supporting tissues of a human maxillary central incisor (H&E × 40 mag) showing many blood vessels in the NVB, some with red blood cells in their lumens.The fibres in the PDL space seem to be in a very close relationship with the NVB but without affecting its continuity.Image courtesy of Dr Teck Hong Oh92

Fig. 3
Fig. 3 The maxillary right central incisor discoloured during OTM but the pulp was normally responsive to CO 2 sensibility testing; subsequent reviews showed PCC and improvement in colour.Periapical radiographs at presentation (top left), five-month review (top centre), and 4.3 years (top right).Photographs on presentation (bottom left) and at five-month review (bottom right).Images courtesy of Dr Vijay John

Fig. 6 93 Fig. 7
Fig. 6 3D reconstructions of different teeth acquired with micro-CT technology depicting the complexity of the apical canal.Image reproduced with permission from Versiani et al., 'Anatomical complexities affecting root canal preparation: a narrative review', Australian Dental Journal, Vol 68, 202393

Fig. 9 Fig. 8
Fig. 9 Male patient (13 years old) undergoing a course of OTM suffered a golf club injury resulting in tooth 11 luxated superolabially, 21 intruded with only incisal edge visible and uncomplicated crown fracture, and 22 intruded approximately half the crown height.a) Pre-operative occlusal radiograph.b) March 1997, teeth repositioned and splinted.c) April 1998, 13-month review showing completed root canal treatment of tooth 21 and remodelled tooth 22 undergoing PCC.d) 23-month review, OTM commenced, tooth 22 showing evidence of transient apical breakdown, orthodontist requested to pause OTM.e) 31-month review showing continued PCC of 22 and apical root remodelling.f, g) 22.5-year review showing advanced replacement resorption of 21, and PCC of 22 with normal apical tissues (panels f and g courtesy of Dr Vijay John)

Fig. 10 A
Fig. 10 A 17-year-old female patient suffered crown fractures on her maxillary central incisors when she was about nine years old; she could not recall the exact trauma history.She had been asymptomatic since the trauma but had noticed that the teeth were discolouring.The teeth were both diagnosed with necrotic infected pulps and asymptomatic apical periodontitis.The treatment option selected was regenerative endodontic procedures for both teeth.a) Pre-operative periapical radiograph, July 2017.b, c) Tooth 11 and tooth 21, review radiographs February 2020.d, e) Review radiographs, October 2021, ten months after commencement of OTM.f, g) May 2023, review radiographs showing satisfactory biological outcomes for both teeth.Images courtesy of Dr Chee Wei Yeap